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Chapter 12 : The Fungal Cell Wall: Structure, Biosynthesis, and Function

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Abstract:

Fungal cell walls are dynamic structures that are essential for cell viability, morphogenesis, and pathogenesis. The wall is much more than the outer layer of the fungus; it is also a dynamic organelle whose composition greatly influences the ecology of the fungus and whose composition is highly regulated in response to environmental conditions and imposed stresses. A measure of the importance of the cell wall can be appreciated by the fact that approximately one-fifth of the yeast genome is devoted to the biosynthesis of the cell wall ( ). Of these approximately 1,200 genes ( ), some are concerned with the assembly of the basic components, others provide substrates for wall materials, and many regulate the assembly process and couple this to environmental challenges. They include genes that encode carbohydrate active enzymes (which can be found in the CAZy database [http://www.cazy.org]) ( ) and include multigene families of chitin and glucan synthases as well as remodeling enzymes such as the glycohydrolases (glucanases, chitinases) and transglycosidases. Many of the building blocks of the cell wall are conserved in different fungal species ( ), while other components of the wall are species-specific, and there is perhaps no part of the cell that exhibits more phenotypic diversity and plasticity than the cell wall.

Citation: Gow N, Latge J, Munro C. 2017. The Fungal Cell Wall: Structure, Biosynthesis, and Function, p 267-292. In Heitman J, Howlett B, Crous P, Stukenbrock E, James T, Gow N (ed), The Fungal Kingdom. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.FUNK-0035-2016
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Figure 1

Structural organization of the cell walls of fungal pathogens. The upper panels show transmission electron micrograph sections of the cell walls, revealing mannoprotein fibrils in the outer walls of , the fibril-free cell wall of an hypha, and the elaborate capsule of . The cartoons (below) show the major components of the wall and current hypotheses about their interconnections. Most fungi have a common alkali-insoluble core of branched β-(1,3) glucan, β-(1,6) glucan, and chitin but differ substantially in the components that are attached to this. In , the outer wall is heavily enriched with highly mannosylated proteins that are mostly attached via glycosylphosphatidylinositol remnants to β-(1,6) glucan and to the β-(1,3) glucan-chitin core. In , typical of many filamentous fungi, mannan chains are of lower molecular weight and are modified with β-(1,5) galactofuran. These mannans are not components of glycoproteins but are attached directly to the cell wall core. The cell wall core polysaccharides of are β-(1,3)-β-(1,4) glucans and are attached to an outer layer of alkali-soluble linear α-(1,3)(1,4) glucan. Conidial walls of have an outer hydrophobin rodlet layer of highly hydrophobic portions (hydrophobins) and a melanin layer; hyphae of have α-(1,3) glucan GM, and galactosaminoglycan (GAG) in the outer cell wall and limited glycosylated proteins. In , an outer capsule is composed of glucuronoxylomannan (GXM) and lesser amounts of galactoxylomannan (GalXM). The capsule is attached to α-(1,3) glucan in the underlying wall, although peptides or other glycans may also be required for anchoring the capsule to the cell wall. The inner wall has a β-(1,3) glucan-β-(1,6) glucan-chitin core, but most of the chitin is deacetylated to chitosan, and some of the chitosan/chitin may be located further from the membrane. also has a layer of melanin whose precise location is not known, but it may be incorporated into several cell wall polysaccharides and may assemble close to the chitin/chitosan layer. cell walls may lack chitin and the outer chain -mannans but retain core -mannan and -mannan modified proteins ( ). Hyphae of and have an outer cell wall layer of α-(1,3) glucan that prevents efficient immune recognition of β-(1,3) glucan in the inner cell wall. (From reference , with permission.)

Citation: Gow N, Latge J, Munro C. 2017. The Fungal Cell Wall: Structure, Biosynthesis, and Function, p 267-292. In Heitman J, Howlett B, Crous P, Stukenbrock E, James T, Gow N (ed), The Fungal Kingdom. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.FUNK-0035-2016
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Figure 2

Synthesis and remodeling of β-(1,3) glucan. Putative sequential or concomitant events in the synthesis and remodeling of β-(1,3) glucan. 1. Synthesis of linear glucan chains (glucan synthase complex composed of a catalytic [GS], activating [Act], and regulating [Reg] subunits). 2. Hydrolysis of glucans. 3. Branching of β-(1,3) glucan. 4. Elongation of β-(1,3) glucan side chains. 5. Cross-linking with branched [β-(1,3)] glucan. GPI-anchored transglycosidase or hydrolases (T) bound to the membrane can act on the polysaccharides in the cell wall space. Panel A provides example. An example of GPI-anchored Gel1 protein involved in the elongation of β-(1,3) glucan inside the cell wall space. Crystal structure of the Gel1 orthologue, Gas2 complex with acceptor and donor oligosaccharides. The enzyme is shown as a ribbon, the glucan binding domain with green strands and orange helices, and the catalytic domain with blue strands and red helices. A gray transparent molecular surface is shown, revealing an elongated groove on the catalytic domain, in which the laminarioligosaccharides (shown as sticks, with yellow carbon atoms) bind. Biochemical organization of a GPI-anchored protein in . The three domains of the GPI anchor are (i) a phosphoethanolamine linker covalently bound to the protein, (ii) a mannan-glucosamine-myo-inositol oligosaccharide, and (iii) a ceramide tail attaching the GPI anchor to the cell membrane. (Data from reference ).

Citation: Gow N, Latge J, Munro C. 2017. The Fungal Cell Wall: Structure, Biosynthesis, and Function, p 267-292. In Heitman J, Howlett B, Crous P, Stukenbrock E, James T, Gow N (ed), The Fungal Kingdom. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.FUNK-0035-2016
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Figure 3

Glucan synthase (Gsc1), chitin synthase (Chs6), and myosin chitin synthase (Mcs1) of are codelivered on the same secretory vesicles and colocalize at bud and hypha tips. mCherry3-Mcs1 (red) and Chs6-GFP3 (green and yellow) colocalized Mcs1 and Chs6 at the bud tip. Scale bar, 2 μm. In the bud is photobleached with a laser, and the codelivery of mCherry3-Mcs1 (red) and Chs6-GFP3 (green) into the photobleached bud is revealed after 5 minutes. Scale bars, 3 μm (left) and 0.5 μm (right). Electron microscopy of secretory vesicles that have been colloidal-gold-labeled with antibodies showing Chs6 and Mcs1 colocalization in a single vesicle. Scale bars: 100 nm. A model for the delivery and secretion of vesicles containing both Chs6 and Msc1 via actin- and microtubule-based cytoplasmic transport systems to the apical cell membrane. After fusion with the apical membrane, the nascent polysaccharide chains of chitin and β-(1,3) glucan are inserted into the cell wall—a process that anchors the synthases , ensuring coordinated synthesis and tethering at the biosynthetically active apical region of the cell. (From Schuster et al. [ ], with kind permission and modification by Gero Steinberg.)

Citation: Gow N, Latge J, Munro C. 2017. The Fungal Cell Wall: Structure, Biosynthesis, and Function, p 267-292. In Heitman J, Howlett B, Crous P, Stukenbrock E, James T, Gow N (ed), The Fungal Kingdom. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.FUNK-0035-2016
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Figure 4

Signaling pathways that regulate cell wall remodeling and cell integrity. Integral, glycosylated, membrane sensors (Wsc family, Mid2, Mtl1, Sho1, and Sln1) detect specific perturbations in the wall and transduce the signal to the downstream pathway elements that feed into MAP kinase cascades. Transcription factors at the bottom of the pathway activate gene expression to promote remodeling of the cell wall architecture to maintain cell integrity. In , Pkc1 is involved in targeting Chs3 to the plasma membrane in response to heat shock, and Rho1 activates the Fks1 subunit of β-(1,3) glucan synthase. Black text denotes proteins; red, ; blue, ; and green, . The fungal pathogen orthologues may not have been fully characterized, and their position in the pathways reflects the paradigm. However, significant rewiring of signaling pathways is evident in ; for example, the role of the CaSko1 transcription factor in response to caspofungin is independent of the Hog1 MAP kinase ( ) but involves the Psk1 PAK kinase. Furthermore, in , there is no evidence of Ste11 activating Hog1 like there is in ( ). In , the Cas5 transcription factor also contributes to the transcriptional response to caspofungin, and there are no Cas5-orthologues in ( ). The CaCek1 MAP kinase is also implicated in cell wall remodeling and is constitutively activated in a null mutant background ( ). Fungal pathogen orthologues of the elements upstream of the MAP kinase cascades are not shown but exist, although the membrane sensors appear to have significantly diverged. Exogenous calcium enters cells primarily through the Cch1/Mid1 channel complexes. A third Ca channel, Fig1, plays a role in Ca transport during mating, but no orthologues of Fig1 have been identified in or . Ca binds to and activates calmodulin (Cmd1), which in turn activates the phosphatase calcineurin, composed of a catalytic (Cna1) and a regulatory (Cnb1) subunit. has two Cna1 isoforms (Cna1/Cmp1 and Cna2/Cmp2). Calcineurin activates the transcription factor Crz1 by dephosphorylation to induce expression of genes that contain calcium-dependent response elements within their promoter sequences. No Crz1 orthologue has been identified in . Some data also suggest that calcineurin has regulatory functions that are independent of Crz1 ( ). Several of the proteins that may be related to this pathway remain unannotated, so putative orthologs have been ascribed but have not been experimentally validated. The pathway can be blocked via FK506 binding to Fpr1 or cylosporin A binding to cyclophilin Cpr1, and both interactions result in calcineurin inhibition. (Adapted from references ).

Citation: Gow N, Latge J, Munro C. 2017. The Fungal Cell Wall: Structure, Biosynthesis, and Function, p 267-292. In Heitman J, Howlett B, Crous P, Stukenbrock E, James T, Gow N (ed), The Fungal Kingdom. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.FUNK-0035-2016
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Figure 5

Chitin synthesis and septum formation in yeasts. Septation involves a protein scaffold that tethers the Chs3p chitin synthase that assembles the chitin ring to Cdc10p of the septin ring complex via Chs4p and Bni4p. The structure of the wild-type septum of (transmission electron microscopy image on right) is shown alongside septum-less yeast cells in a conditional mutant (middle transmission electron microscopy image) and salvage septa (transmission electron microscopy image on left) made in the same mutant strain after stimulation of the cell wall salvage pathways by growth in the presence of calcium ions and calcofluor white. (Reused from reference under CC BY 4.0).

Citation: Gow N, Latge J, Munro C. 2017. The Fungal Cell Wall: Structure, Biosynthesis, and Function, p 267-292. In Heitman J, Howlett B, Crous P, Stukenbrock E, James T, Gow N (ed), The Fungal Kingdom. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.FUNK-0035-2016
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Figure 6

Recognition of human fungal pathogens. PAMP-PRR interactions for fungal cell recognition are shown as described in the text. Interactions with CLRs (C-type lectins), TLRs (Toll-like receptors), NLRs (Nod-like receptors), and a range of other receptors are shown in the purple boxes along with the relevant fungal PAMPs and examples of organisms for which given PRR-PAMP recognition phenomena have been described.

Citation: Gow N, Latge J, Munro C. 2017. The Fungal Cell Wall: Structure, Biosynthesis, and Function, p 267-292. In Heitman J, Howlett B, Crous P, Stukenbrock E, James T, Gow N (ed), The Fungal Kingdom. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.FUNK-0035-2016
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Figure 7

Recognition and avoidance of the recognition of chitin by plant pathogens. The detection of fungal chitin is used to trigger PAMP-mediated immunity in plants. To counter this, plant pathogenic fungi have evolved a range of mechanisms to avoid detection, including the following. The liberation of chitin fragments by host chitinase attack can activate host immunity. Countering this, some phytopathogens secrete effectors that block access to chitinase or inhibit chitinase activity. Fungal LysM-type effectors block recognition either by tight binding to prevent engagement with the host PRR or by interfering with host receptor dimerization. The synthesis of an outer cell wall layer of α-(1,3) glucan (as in certain human pathogenic species) prevents chitinase action and access to inner cell wall PAMPs. Some fungal pathogens convert, to a greater or lesser extent, chitin into chitosan by inducing chitin deacetylases. This modified form of chitin is a poor substrate for chitinase and only weakly induces plant immune recognition. (From Bart Thomma with permission [adapted from reference ]).

Citation: Gow N, Latge J, Munro C. 2017. The Fungal Cell Wall: Structure, Biosynthesis, and Function, p 267-292. In Heitman J, Howlett B, Crous P, Stukenbrock E, James T, Gow N (ed), The Fungal Kingdom. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.FUNK-0035-2016
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